Fatty acid signatures connect thiamine deficiency with the diet of the Atlantic salmon (Salmo salar) feeding in the Baltic Sea

Abstract

Thiamine (vitamin B1) deficiency in salmonids related to a lipid-rich fish diet causes offspring mortality in the yolk-sac fry phase. A low free thiamine (THIAM) concentration in eggs is an indication of this syndrome. Thiamine deficiency of salmon (Salmo salar) feeding in the Baltic Sea, called M74, was connected to the principal prey fish and feeding area using fatty acid (FA) signature analysis. The FAs of feeding salmon from two areas of the Baltic Sea, the Baltic Proper (57°10′ 19°30′) and the Bothnian Sea (61°30′ 20°00′) in 2004, reflected the principal prey species in these areas, sprat (Sprattus sprattus) and herring (Clupea harengus), respectively. Arachidonic acid (ARA, 20:4n-6) and 18:1n-7 indicated dietary herring, 18:1n-9 dietary sprat and 14:0 feeding in the Baltic Proper. The muscle FA profile of non-M74 female spawners of the River Simojoki in a year (1998) with a moderate M74 incidence and salmon of a non-M74 year (2004) reflected herring FAs, whereas the FAs in the M74 year and specifically in M74 females displayed characteristics of sprat. In the M74 year, the THIAM concentration had the strongest positive correlation with the proportion of muscle ARA, and the strongest negative correlations with 14:0 and the ratios 18:1n-9/ARA and 14:0/ARA. Thus, ARA along with 14:0 and these ratios were the most sensitive FA indicators of the dietary species and origin of the M74 syndrome. Despite the pre-spawning fasting, tissue FA signatures were consequently able to connect dietary sprat in the Baltic Proper with thiamine deficiency in Baltic salmon.Electronic supplementary materialThe online version of this article (10.1007/s00227-018-3418-8) contains supplementary material, which is available to authorized users.

Deficiency syndromes in top predators associated with large-scale changes in the Baltic Sea ecosystem

“…The second hypothesis is that M74 arise when salmon eat proportionally more smallsized sprat compared to large sprat and herring [7,26]. The small sized sprat have relatively low concentrations of thiamin per energy content compared to other clupeids [6,9,27]. Yet another hypothesis is that the prey fish of salmon (sprat and herring) contain a thiamin degrading enzyme called thiaminase reducing the uptake of thiamin [30,31].…”

“…Hence, the changes in abiotic conditions and consequent changes in the species composition and size distribution of primary producers, that have occurred in the Baltic Sea, could have constrained the flow of thiamin from lower to higher trophic levels of the system. However, not only bottom-up factors such as nutrients seem to play a role since it has also been shown that M74 incidence is correlated with the stock size of sprat [7,26], with the suggested cause of M74 being salmon consumption of small individuals with a relatively low thiamin concentration per unit of fat content [6,27]. Our data supports that M74 is most severe during periods with high abundance of planktivorous fish but correlations occur, not only for sprat, but also for herring.…”

“…Hence, our main hypothesis is that M74 outbreaks are associated to changes in the food web structure. These changes would then affect the quality and transfer of food items in terms of fatty acids, vitamins and pigments from the producers at lower trophic levels to higher trophic levels [6,27,46,47] but this latter hypothesis is not within the scope of this study. Hence, the lack of an understanding of the abiotic and biotic conditions during M74-outbreaks calls for an analysis of whether large-scale changes at multiple levels of the ecosystem affect the occurrence of deficiency syndromes among top predators.…”

“…When salmon are accessing thiamin from the diet (i.e. mainly clupeids) it has also been argued that the risk of thiamin deficiency increases when consumption of juvenile sprat is high since these contain a lower supply of thiamin per unit of energy [6,9,27]. Finally, during the transfer of thiamin from clupeids to salmon there is also a risk of thiamin breakdown if the enzyme thiaminase is present [30,31] but there are no studies that evaluate how different enzyme activities change the overall transfer of thiamin to salmon given the thiamin concentration available in the prey.…”

“…However, the diet of salmon had a lower proportion of sprat during years with a high incidence of M74 in the 1990s compared to a low-incidence period in 1959-1962 [25,26]. Recently, thiamin deficiency syndromes in salmon were also connected to feeding area and type of prey by fatty acid signature analysis [27]. In the Great Lakes, the thiamin deficiency syndrome EMS (early mortality syndrome) has been proposed to be related to the introduction of a thiaminase-rich prey species, alewife (Alosa pseudoharengus) [28].…”